High‐latitude kelps and future oceans: A review of multiple stressor impacts in a changing world

Abstract Kelp forests worldwide are threatened by both climate change and localized anthropogenic impacts. Species with cold‐temperate, subpolar, or polar distributions are projected to experience range contractions over the coming decades, which may be exacerbated by climatic events such as marine heatwaves and increased freshwater and sediment input from rapidly contracting glaciers. The northeast Pacific has an extensive history of harvesting and cultivating kelps for subsistence, commercial, and other uses, and, therefore, declines in kelp abundance and distributional shifts will have significant impacts on this region. Gaps in our understanding of how cold‐temperate kelp species respond to climate stressors have limited our ability to forecast the status of kelp forests in future oceans, which hampers conservation and management efforts. Here, we conducted a structured literature review to provide a synthesis of the impacts of multiple climate‐related stressors on kelp forests in the northeast Pacific, assess existing knowledge gaps, and suggest potential research priorities. We chose to focus on temperature, salinity, sediment load, and light as the stressors most likely to vary and impact kelps as climate change progresses. Our results revealed biases in the existing literature toward studies investigating the impacts of temperature, or temperature in combination with light. Other stressors, particularly salinity and sediment load, have received much less focus despite rapidly changing conditions in high‐latitude regions. Furthermore, multiple stressor studies appear to focus on kelp sporophytes, and it is necessary that we improve our understanding of how kelp microstages will be affected by stressor combinations. Finally, studies that investigate the potential of experimental transplantation or selective cultivation of genotypes resilient to environmental changes are lacking and would be useful for the conservation of wild populations and the seaweed aquaculture industry.


| INTRODUC TI ON
Kelps are large brown macroalgae of the order Laminariales which form extensive underwater forests and have a widespread distribution across temperate and polar coastlines (Smale, 2019). These organisms are of fundamental importance to the coastal systems in which they occur and provide diverse ecological and economic benefits. The biogenic habitat they provide constitutes one of the most productive ecosystems on the planet, supports a rich associated biodiversity, and provides critical ecosystem services, including erosion control, nutrient cycling, and the provision of shelter and nursery areas for socioeconomically important fish species and multiple life stages of other marine species (Siddon et al., 2008;Smale et al., 2013;Steneck & Johnson, 2013;Teagle et al., 2017;Wernberg et al., 2019).
Kelp forests worldwide are coming under threat from the combined pressures of global climate change and localized anthropogenic impacts. Kelp forests are highly dynamic systems that are sensitive to changes in the physical, chemical, or biological characteristics of their environment (Smale et al., 2013). Point stressors such as coastal hardening (Marzinelli et al., 2011;Mayer-Pinto et al., 2018), eutrophication (Strain et al., 2014;Tegner et al., 1995), herbivory (McPherson et al., 2021;Rogers-Bennett & Catton, 2019), and changes in physicochemical factors (Lind & Konar, 2017;Schoch & Chenelot, 2004;Vettori et al., 2020) may lead to altered kelp forest function, changes in associated biota, localized declines in kelp abundances, and even local extinctions (Smale, 2019). Globally, rising sea surface temperatures and an increased frequency of marine heatwaves have led to widespread changes in kelp distributions Gordillo et al., 2022;Martínez et al., 2018;Smale et al., 2019;Tait et al., 2021), including range expansions for cold range edge species and range contractions for warm range edge species (Smale, 2019), with knock-on effects for associated biodiversity and trophic exchanges (Schiel et al., 2014). These impacts are particularly pronounced in polar, sub-polar, and cold-temperate regions.
Rising sea surface temperatures have resulted in poleward shifts in species ranges, particularly for cold-temperate species (Goldsmit et al., 2021;Wilson et al., 2019). Rates of warming in the Arctic are approximately four times higher compared to the rest of the globe, a phenomenon known as polar amplification (Rantanen et al., 2022). Therefore, it is likely that kelp species with current cold-temperate, subpolar, or polar distributions will experience significant range contractions over the coming decades, which may be exacerbated by extreme climatic events such as marine heatwaves, potentially to the point of local extirpations or global extinctions Wilson et al., 2019). Additionally, polar, subpolar, and cold-temperate regions are susceptible to the effects of glacial melt, which contributes to decreased salinities and increased sedimentary deposits at glacial outflows, both of which have been shown to impact kelp physiology and the provision of ecosystem services (Lind & Konar, 2017;Traiger & Konar, 2017;Vettori et al., 2020). Glacial contraction is likely to be exacerbated by increasing sea surface temperatures, resulting in a higher rate of freshwater and sediment deposition into coastal environments.
Although ongoing climate change will also result in pH effects, including ocean acidification, research suggests that these changes will have minimal to no impact on the physiology of kelp species (Fernández et al., 2015;Roleda et al., 2012). A deeper understanding of the dynamics of kelp forests in these cold-water regions is fundamental to developing predictions of kelp functioning and distributions under future ocean conditions. The northeast Pacific, and Alaska in particular, is likely to experience significant shifts in species distributions under warming conditions. This region represents the northern limit of distribution for several seaweed species which occur mainly to the south of Alaska (Stekoll, 2019), including Alaria marginata, several species of Laminaria and Saccharina, and the canopy-forming kelps Macrocystis pyrifera, Nereocystis luetkeana, and Eualaria fistulosa (Stekoll, 2019).
Humans have harvested kelp in the northeast Pacific since time immemorial, and current kelp harvest supports important subsistence and commercial food products and fisheries. N. luetkeana, for example, is harvested for processing into commercially available food products, and M. pyrifera is harvested as part of the roe-on-kelp fishery (Stekoll, 2019). Recently, there has been increasing interest and investment in the commercial cultivation of a few species, including Saccharina latissima and A. marginata (Stekoll et al., 2021). This is an emerging and potentially highly lucrative industry that is likely to experience significant impacts from the combined effects of global and local stressors on kelp ecology, physiology, and distribution.
Up to this point, much of the research involving the susceptibility of kelps to climate change and anthropogenic stressors has been focused on the impacts of rising sea surface temperatures and marine heatwaves, and a number of comprehensive reviews exist in this regard, particularly from the North Atlantic (Smale, 2019;Smale et al., 2013Smale et al., , 2019. Comparatively few reviews have been concerned with the northeast Pacific region (but see Hollarsmith et al., 2022).
More recently, there has been increasing interest in the impacts of anthropogenic stressors on the microscopic stages of kelps, heretofore considered the "black box" of the kelp life cycle due to the difficulties involved in taking in situ measurements (Coelho et al., 2000;Martins et al., 2023;Veenhof et al., 2022); however, there is much left to be done in this regard and full consideration of how this may impact the economic benefits and environmental services of kelp forests is lacking.
This review aims to provide a synthesis of the potential impacts of multiple climate-related stressors on kelp forests in Alaska and the northeast Pacific. We review the literature on responses of coldtemperate, subpolar, and polar kelp species of this region to climaterelated stressors, considering impacts on both the macroscopic and microscopic stages of the life cycle and assessing whether the stressors in question have been tested singly or in combination.
Subsequently, we identify key patterns emerging from the literature and consider the implications with regard to the persistence of coldadapted kelps under future ocean conditions. Finally, we identify the main knowledge gaps arising from this review and suggest potential research priorities over the coming decade.

| RE VIE W ME THODS
The studies included in this review were selected through a systematic literature search in Scopus, targeting climate and anthropogenic stressors likely to have the greatest impact on kelps in Alaska and the northeast Pacific region, defined here as the region between 30°N and 60°N, and between 120°W and 180°E (Table 1). As water temperatures increase, glacial contraction will decrease salinity and increase sediment load, which in turn attenuates light penetration.
Temperature, salinity, sediment, light, and UV were, therefore, considered to be most likely to vary over the coming decades as a result of ongoing climate change and to directly impact kelp species, and were therefore selected a priori as stressors of interest. The genera Saccharina, Alaria, Nereocystis, Eualaria, and Macrocystis were considered to have the most ecological and commercial importance in the northeast Pacific region ( Figure 1) and were therefore selected a priori as genera of interest. Our initial search resulted in a total of 1187 results, which were subsequently screened to determine their suitability for inclusion in this study. We excluded: (i) duplicate results, (ii) results that were outside of the scope of this review, (iii) studies conducted outside of the temperate to polar latitudes of the Northern Hemisphere, and (iv) reviews and meta-analyses. Kelp populations outside of the region of focus are subject to different biological and environmental pressures, such as interspecific interactions and climatic patterns, and were therefore considered to be out of scope. After screening, a total of 193 studies were included in this review (Data S1).
Each result was individually analyzed and assigned specific keywords or combinations of keywords (Table 2) according to the following criteria: (i) species of interest, (ii) stressor of interest, (iii) experiment type, (iv) single versus multiple stressor design, (v) stressor interactions, (vi) individual stressor effects, (vii) kelp life stage, (viii) response variable, and (ix) geographical region. As very few existing studies consider A. marginata, the north Atlantic/Arctic species A. esculenta was included in this review as the closest extant congener. This is also a cold-adapted subcanopy species and is therefore expected to have similar ecological characteristics and will respond to climate variability in a similar way. These data were subsequently visualized in order to elucidate broad patterns and biases across this pool of studies.

| General trends and patterns in the literature
Approximately 45% of the studies identified in this review are con- Saccharina latissima has a similarly widespread distribution in temperate, polar, and subpolar regions of the northern hemisphere (Nielsen et al., 2014). Additionally, there is a long history of the commercial harvest of S. latissima in both the Pacific and Atlantic Oceans (Peteiro et al., 2016). Comparatively few studies focus on other species of interest in Alaska and the NE Pacific, such as A. marginata or N. luetkeana (10%). Most studies involving the genus Alaria focus on Alaria esculenta (14%), but even these are limited in number compared to S. latissima and M. pyrifera, as previously described. Both A. marginata and N. luetkeana are ecologically and commercially relevant in the NE Pacific-the latter is a major canopy-forming species along Pacific coastlines and is harvested for commercial use (Springer et al., 2010;Stekoll et al., 2006), while A. marginata is a significant component of the mariculture industry in this region (Stekoll, 2019).
Approximately 21% of studies specifically investigate the responses of early life stages of kelps to stressor impacts ( Figure 3a).
As previously mentioned, these kelp microstages are difficult to study in the field (Coelho et al., 2000;Martins et al., 2023;Veenhof et al., 2022), and it is therefore only logical that most studies would focus on the sporophyte stage, as wild populations are readily located and present throughout most of the year. The majority of studies measure physiological responses to stress, including growth, survival, and reproductive responses.
In general, slightly more studies consider the impacts of multiple stressor systems (54%) than the impacts of single stressors (46%) ( Figure 3b). The overwhelming majority focus on temperature (60%).
This reflects climate priorities, as a rise in sea surface temperature and the frequency of marine heatwaves is likely to be the major climate-related impact on marine systems over the coming decades A total of 64 studies (~33%) involved field-based approaches, and only 17 studies (~9%) utilized computer-based modeling approaches ( Figure 4a). Across these categories, we observed a fairly even split between multiple-stressor and single-stressor approaches ( Figure 4b).

| Temperature
A total of 117 studies consider the impacts of temperature either in isolation or in conjunction with other stressors. Of these, 73% report negative biological effects as a result of increasing temperature, while 11% report positive biological effects. This apparent discrepancy is a consequence of different temperature ranges being tested across different studies. In general, any variation in temperature outside of the optimum range for a given species-whether in colder or warmer conditions-will result in negative effects.  Lab-based Modelling approach Field-based Temperature tolerance ranges for kelp sporophytes vary by species; for example, S. latissima sporophytes can survive temperatures between −1.5 and 23°C, while A. esculenta has a slightly lower upper survival limit of 21°C (Dieck, 1993). Increasing temperature beyond the optimum for a given species has a variety of impacts, including decreasing photosynthetic yield (Niedzwiedz et al., 2022), overall individual survival, and biomass and tissue strength in S. latissima , quality and commercial value in S. latissima and M. pyrifera (Lowman et al., 2022;, phenotypic plasticity in N. luetkeana (Supratya et al., 2020), and spore development and settlement in M. pyrifera (Le et al., 2022). On the contrary, a rise in sea surface temperature is likely to favor kelp populations at the lower threshold of their thermal tolerances, resulting in overall positive biological effects and range expansions into northern regions by cold range edge species (Smale, 2019 (2017) report that the early life-history stages of Alaskan kelps experience significant impacts at elevated temperatures, including decreases in spore settlement concentration, spore germination, and germ tube growth. However, some degree of settlement and initial growth was still observed, suggesting that kelp microstages may be resilient to thermal stress to a certain extent (Lind & Konar, 2017). In S. latissima gametophytes, temperature has been shown to modulate the expression of sex-biased genes, with female individuals exhibiting more marked responses than males-this may have implications for reproductive success of this species in a warming environment . Responses of kelp microstages to thermal stress vary across populations within a species; for example, Hollarsmith et al. (2020) report developmental failure at the egg and sporophyte stages of M. pyrifera from high-latitude California populations, whereas specimens from low-latitude populations are able to produce sporophytes at elevated temperatures. This suggests that certain populations within a given species may exhibit a degree of thermal resilience, which would have important implications for the conservation of cold-adapted species.

F I G U R E 2
A warming ocean will likely result in significant changes in distribution for a number of kelp species, specifically range contractions for cold-adapted species and range expansions for warm-adapted species (Martínez et al., 2018). For any given species, the impacts of warming are likely to be more pronounced in trailing edge populations, which exist close to their thermal survival limits (Tait et al., 2021).
Therefore, in colder regions, elevated temperatures are likely to disproportionately favor species with more temperate distributions.
For example, S. latissima sporophytes from Norway exhibit an increase in growth and maximal yield for photosystem II fluorescence (Li, Monteiro, et al., 2020), and gametophytes of this species from this region are able to produce sporophytes at 15°C, while gametophytes of A. esculenta from the same region do not produce sporophytes at the same temperature (Park et al., 2017). Furthermore, it has been shown that sporophytes of S. latissima from Norway show no decrease in photosynthetic yield at 15°C (Andersen et al., 2013) and still have a measurable, albeit greatly reduced, photosynthetic yield at 20°C (Park et al., 2017), while sporophytes of A. esculenta have a photosynthetic yield of zero at the latter temperature (Park et al., 2017). The spores and gametophytes of both M. pyrifera and N. luetkeana experience significant negative impacts under elevated temperatures and hyposaline conditions, including decreased spore settlement concentration and germ tube growth, but these effects are not as pronounced for Eualaria fistulosa, a less widely-distributed species (Lind & Konar, 2017). Furthermore, for M. pyrifera the upper thermal threshold for spore and germling development has been reported to be between 21.7 and 23.8°C (Le et al., 2022). This suggests that species such as M. pyrifera and S. latissima may experience range expansions into higher latitudes, whereas more cold-adapted species such as A. esculenta and A. marginata will experience range contractions and may disappear from areas at their lower distribution limits. It is important to note, however, that species distributions will also be affected by oceanographic and hydrographic factors, and are therefore not simple to predict.
Heatwave scenarios and extended periods of elevated tempera- Overall, it appears that increasing temperature beyond the optimum will result in reduced germination success and growth rates for kelp microstages (Hollarsmith et al., 2020;Lind & Konar, 2017), species are likely to experience increases in their global distributions (Martínez et al., 2018;Smale, 2019;Tait et al., 2021). In the region of focus of this paper, this suggests that A. marginata and N. luetkeana are more likely to experience range contractions, whereas M. pyrifera and S. latissima may expand their ranges. There is currently a lack of information regarding how E. fistulosa responds to changes in temperature, and therefore predictions of how this species will fare in future oceans are less straightforward. Long-term thermal stress increases the susceptibility of kelp populations to other stressors, and so the temperature is likely to interact with other climate-related stressors in complex ways.

| Salinity
Salinity is considered as a stressor in only 26 (14%) of the studies included in this review. Changes in environmental salinity are usually associated with estuarine habitats and riverine influences, so salinity is not generally thought of as a climate stressor. However, a rise in global temperatures is likely to increase the rate of glacial melt and lead to changes in salinity in glacially-influenced environments, particularly in polar and subpolar regions. Furthermore, precipitation during winter will be more likely to fall as rain rather than snow, resulting in more rapid runoff and longer periods of consistent freshwater input into the coastal environment, which will have an impact on the ecology of high-latitude kelp forests.
Hyposaline conditions (< 20 psu) are associated most often with reduced rates of photosynthesis (Karsten, 2007;Li, Monteiro, et al., 2020;Monteiro, Li, et al., 2019;Spurkland & Iken, 2011b) and the loss of photosynthetic pigments in A. esculenta, S. latissima, and L. solidungula (Karsten, 2007). However, other studies have reported declines in S. latissima sporophyte growth rates (Monteiro et al., 2021), and gametophyte growth rates and spore settlement of Overall, responses to changes in salinity appear to be speciesspecific (Bruhn et al., 2017) and population-specific within a given species (Monteiro, Li, et al., 2019). Salinity tends to be much more variable than temperature along coastlines, with localized extremes associated with estuaries and glacial input, and there is evidence that specific populations have adapted to these conditions and exhibit genetic and phenotypic differences (Møller Nielsen et al., 2016;Spurkland & Iken, 2012). This fact suggests that certain kelp populations may be more resilient to climate-induced changes in salinity, and bears further investigation.

| Light and UV
The impacts of irradiance are considered from two major perspectives in the literature reviewed here: the effects of photosynthetically active radiation (PAR, 400-700 nm) were considered in a total of 64 studies (33%), and the effects of ultraviolet radiation (UV-A and UV-B, 100-400 nm) were considered in a total of 29 studies (15%).
Exposure of marine organisms in polar regions to both these types of radiation is expected to increase in frequency and duration over the coming decades due to continued stratospheric ozone depletion over the poles (Müller et al., 2012). However, there is evidence that increased sediment load protects kelp forests from higher light intensities to a degree (Roleda et al., 2008), and therefore an increased rate of glacial contraction due to ongoing climate change may serve to mitigate increases in both PAR and UV radiation.
However, intensities of PAR beyond optimal levels and increasing intensity of UV wavelengths also have negative effects on kelp species, including cellular, enzymatic, and molecular damage, decreased growth rates, changes in DNA expression, and photo-oxidative stress in S. latissima (Bruhn & Gerard, 1996;Heinrich et al., 2012Heinrich et al., , 2015Roleda et al., 2006b) and photoinhibition in M. pyrifera and N. luetkeana (Clendennen et al., 1996;Mabin et al., 2019;Poulson et al., 2011). The majority of these effects are the result of lightinduced damage to photosystems I and II and chloroplast membranes (Bruhn & Gerard, 1996;Holzinger et al., 2011). However, in many cases, the magnitude of these effects varies by population and depends on exposure time and specific wavelength (Bruhn & Gerard, 1996;Roleda, 2009;Roleda et al., 2006a).
Specifically, studies have found that increasing intensity of PAR (>20 μmol/m 2 /s) causes photoinhibition in spores of S. latissima, and

UV-A and UV-B wavelengths have a significant additional effect;
spores did not recover from exposure times of over 8 h to UV-A and over 4 h to UV-B (Roleda et al., 2005;Wiencke et al., 2000Wiencke et al., , 2004. This loss of zoospore viability is thought to be the result of photodamage to both DNA and the photosynthetic apparatus (Wiencke et al., 2000). These impacts are often population-specific, with evidence of ecotypic differences across the distribution range of particular species. For example, Müller et al. (2008) report that while UV-B consistently inhibits spore germination in two separate populations of S. latissima, the effects of UV-A vary by population and are modulated by temperature. Gerard (1990) shows ecotypic differences in the photosynthetic capacity and photoacclimation responses of S. latissima (as Laminaria saccharina) from three different populations growing in different ambient light regimes. This suggests that certain species or populations may be quicker to adapt to changes in light intensity or exposure time than others (Palacios et al., 2021), which has implications for the ecology and persistence of cold-temperate kelps in a changing climate.
Overall, kelp microstages appear to be more sensitive to irradiance levels than the sporophyte stage, and variations in light penetration will impact the timing of sporulation and germination of both spores and gametophytes (Graham, 1996;Huovinen et al., 2000;Makarov & Voskoboinikov, 2001;Müller et al., 2009;Roleda et al., 2005Roleda et al., , 2006aWiencke et al., 2000Wiencke et al., , 2004. Light intensities above optimal levels result in photodamage and decreased growth rates in sporophytes (Bruhn & Gerard, 1996;Clendennen et al., 1996;Heinrich et al., 2012;Mabin et al., 2019;Poulson et al., 2011;Roleda et al., 2006b), while light intensities below optimal levels will also lead to decreased growth rates and higher mortalities (Bonsell & Dunton, 2018;Kavanaugh et al., 2009;Mabin et al., 2019;Spurkland & Iken, 2011b). Regions of the northeast Pacific coastline that are subject to significant glacial influence will experience decreased light penetration in the coming years as climate change progresses and the rate of glacial melt increases (Roleda et al., 2008). Kelp forests in these areas are likely to exhibit reduced abundances and growth rates as a result of impacts on photosynthesis and the timing of sporulation and germination for microstages. Susceptibility to variations in light intensity varies both by species and by population (Bruhn & Gerard, 1996;Gerard, 1990;Palacios et al., 2021;Roleda, 2009;Roleda et al., 2006a)-for example, S. latissima displays significant ecotypic differences across its distributional range and may be better able to adapt to these changes.

| Sedimentation
Only 11 studies (6%) consider the impacts of sediment load either directly or indirectly. This can be a challenging environmental variable to investigate; the type and degree of sedimentation to which kelp beds are exposed tends to be a highly localized phenomenon, and sediment dynamics are difficult to accurately recreate in labbased studies. However, sedimentation does have a number of impacts on kelp beds and is relevant in areas subject to glacial and riverine influence. Glaciers discharge freshwater and terrestrial sediments into coastal environments, both of which alter local conditions in a number of ways and impact the structure and function of kelp forests (Spurkland & Iken, 2011a). Increased sediment load attenuates light penetration, thereby affecting photosynthesis and productivity, and also physically impacts kelp through sediment scour (Aumack et al., 2007;Picard, Johnson, Ferrario, et al., 2022).
The evidence suggests that in the short term, cold-temperate kelp species are able to acclimate to and recover from increased sediment loads in the water column. Roleda and Dethleff (2011) show that short-term increases in sediment loads have no impact on S. latissima, while Shaffer and Parks (1994) report that a landslide in Puget Sound initially reduced abundances in beds of N. luetkeana, which subsequently appeared to recover. Transient increases in sedimentation may even have positive effects by providing some degree of UV attenuation and protecting kelp tissues from photodamage (Roleda et al., 2008).
On the contrary, consistent and long-term increases in sedimentation are associated with kelp bleaching, loss of photosystem II function, and tissue decay, all of which can be attributed to increased light attenuation under higher sediment loads (Roleda & Dethleff, 2011).
Sediment scour is particularly influential in determining the survival and success of kelp microstages, especially during settlement and attachment to the substratum. The literature indicates that scouring effects and burial strongly inhibit spore germination in S. latissima and A. esculenta , gametophyte survival in S. latissima (Traiger & Konar, 2017), and sporophyte germination and growth in M. pyrifera, S. latissima and A. esculenta (Muth et al., 2021;Zacher et al., 2016). Interestingly, however,  and Picard, Johnson, Ferrario, et al. (2022) show that increased sediment loads actually improve spore attachment in S. latissima, and suggest that this is due to the chemotactic responses of spores to nutrients carried by sediment granules.
Responses to sedimentation are therefore complex and likely to be species-specific. Indeed, S. latissima is considered to be relatively tolerant to variations in turbidity when compared to A. esculenta or N. luetkeana Traiger & Konar, 2017), and may gain a competitive advantage from an increase in sediment loads in glacially-influenced waters.
In general, increased sediment load will lead to decreased light penetration and, consequently, decreased growth rates and tissue decay in sporophytes. Scouring effects and burial by increased sediment loads will severely impact the survival and success of kelp microstages, by inhibiting spore germination, gametophyte survival, and sporophyte germination. As previously discussed, glacially-influenced areas will experience increased turbidity and therefore increased scouring and decreased light penetration under future climate conditions. These scouring and shading effects are likely to impact kelp abundances in these areas by directly affecting the growth of sporophytes and the survival of microstages. Once again, S. latissima has been shown to be relatively tolerant to variations in turbidity and is likely to persist in these areas, potentially outcompeting species such as A. marginata and N. luetkeana.

| Nutrients
The influence of nutrient supply on kelps was considered in 29 (15%) of the studies included in this review. Nutrient availability can be a limiting factor for kelp growth and plays a role in determining the limits of distribution of some species (Strong-Wright & Taylor, 2022).
However, nutrient fluxes tend to interact significantly with other environmental conditions; for example, nutrient availability varies substantially by temperature, and we have already discussed how nutrients may be carried by sediment granules . Indeed, nutrient supply is often inextricably linked to large-scale, complex climatic processes (Dayton et al., 1992;Ladah & Zertuche-González, 2022). The impacts of ongoing climate change on these processes are not straightforward to determine, and therefore it is difficult to predict how nutrient supply might influence kelp forests in the near future. Furthermore, other anthropogenic activities-such as agriculture-often impact nutrient availability on a local scale, and, therefore, nutrient supply tends to be highly spatially and temporally variable.
The influence of nutrient supply on kelp forests is complex and tends to depend on the nature of the ecosystem and the types of interspecific interactions present. For example, an increase in nutrient supply may favor fast-growing filamentous algal species rather than large habitat formers such as kelps, and therefore eutrophication tends to drive shifts from kelp forests to less productive turf reef systems (Moy & Christie, 2012). On the contrary, studies have recorded sharp declines in kelp abundances associated with decreased nutrient availability as a result of changes in large-scale ocean processes (Berry et al., 2021;García-Reyes et al., 2022). Stekoll et al. (2021) suggest that nutrients added to the water in the late summer may improve M. pyrifera survival through the dark winters in southeast Alaska. An increased nutrient supply has been shown to result in higher growth rates (Dean & Jacobsen, 1984;Jevne et al., 2020) and higher thermal tolerances in several species Gerard, 1997;Schmid et al., 2020), while nitrate limitation decreases photosynthetic capacity in M. pyrifera (Umanzor et al., 2021).
Nutrients also play a significant role in controlling the kelp life cycle. Carney and Edwards (2010)

| Multiple stressor systems and impacts
Once again, most of the studies included in this review that consider more than one stressor included temperature.  Gordillo et al. (2022) report that losses in biomass for cold-adapted kelp species cultured under continuous darkness are enhanced when the temperature is increased from 3 to 8°C.
Additionally, after being cultured in continuous darkness at 8°C, A. esculenta and S. latissima are unable to resume growth and photosynthesis upon illumination (Gordillo et al., 2022). It is important to note, however, that the conditions as described in Gordillo et al. (2022) are extremes, and kelp forests in Alaskan waters are unlikely to experience total darkness as a result of increased turbidity. Furthermore, temperature-induced loss of M. pyrifera during a marine heatwave event was found to be more significant in turbid conditions (Tait et al., 2021). It is thought that this phenomenon is the result of metabolic stimulation under elevated temperatures, resulting in kelps metabolizing their storage compounds more quickly and being unable to replace them in darkness or under reduced light conditions (Li, Scheschonk, et al., 2020). This has significant implications for the survival of kelp forests through and beyond the polar winter under future climate scenarios. Certain species, such as S. latissima, may compensate for metabolic stimulation by repressing transcriptomic activities related to energydemanding processes under elevated temperature conditions (Li, Scheschonk, et al., 2020). Indeed, this species exhibits significantly altered gene expressions at higher temperatures and even more so at higher temperatures under high light intensities, suggesting that this combination causes the most metabolic stimulation (Heinrich et al., 2015).
Changes in light intensity may compensate for temperatureinduced stress in kelps and vice-versa. Increased light during the reproduction and development of microstages of A. esculenta has been shown to improve sporophyte survival at elevated temperatures (Martins et al., 2022). Conversely, a moderate increase in temperature has been shown to decrease photoinhibition under high light intensities and improve the recovery of photosynthesis in A. esculenta and S. latissima (Roleda, 2009 Gerard, 1997;Schmid et al., 2020).
Few studies report interactions between temperature and salinity. However,  and Monteiro, Li, et al. (2019) show that temperature modulates the impacts of a hyposaline environment on S. latissima, as genes related to photosynthesis and pigment synthesis are repressed at low temperatures in hyposaline conditions. This phenomenon appears to be ecotypespecific, as temperate populations exhibit the most transcriptomic changes at low temperatures and hyposaline conditions, while coldadapted populations exhibit most changes at higher temperatures (Monteiro, Li, et al., 2019). Therefore, certain populations may be resilient to future changes in temperature and salinity, and approaches to kelp conservation may benefit from the identification and propagation of specific genetic profiles within the wider species distributions.
Kelp microstages are once again particularly vulnerable to combined changes in salinity and temperature. Lind and Konar (2017) report decreased spore settlement and gametophyte growth for both N. luetkeana and S. latissima under elevated temperatures and hyposaline conditions, although both species exhibit some resilience to these stressors. In A. esculenta, the germination capacity of spores is reduced under low salinities and extreme temperatures, but the temperatures tested thus far are probably not ecologically realistic under future climate scenarios, and the species appears to be mostly resilient to differing salinities under ecologically relevant temperature conditions (Fredersdorf et al., 2009).

| CON CLUS IONS AND RECOMMENDATIONS
In this review, we have given an overview of the state of current knowledge regarding the impacts of climate-related stressors on high-latitude kelp species, as well as interpretations of how these kelp forests might respond to a changing ocean over the coming decades. It is clear that the main focus of the field thus far has been on changing temperatures and ocean warming, and while some questions remain, we now have a reasonable understanding of how this will impact kelp forest distributions and ecology going forward.
Other climate-related stressors have not received a similar level of attention, and our understanding of these is still lacking. For polar and subpolar regions in particular, further research is needed on the impacts of changing salinities and sedimentation rates on kelp species in areas subject to glacial influence. Most studies considered in this review were laboratory-based, and therefore more work needs to be focussed on field-based and modeling approaches.
An increasing number of studies are considering how combinations of multiple stressors will impact cold-temperate kelp ecology (Gordillo et al., 2022;Heinrich et al., 2015;Li, Scheschonk, et al., 2020;Tait et al., 2021;Umanzor et al., 2021). This is a much more realistic representation of natural systems, and we would recommend that future investigations consider more varied combinations of stressors. In particular, salinity and sediment load are likely to vary in conjunction with one another in glacially-influenced regions, and studies considering these two stressors in combination are lacking. Temperature is most frequently included in multiple stressor studies, but few investigations combine temperature with variations in salinity (Monteiro et al., 2021) or sedimentation-these combinations would provide invaluable information regarding the future of kelp forests in polar and subpolar regions in a warming climate.
Furthermore, while the studies in this review were nearly evenly split between those considering the sporophyte stage and those considering kelp microstages, the multiple stressor studies specifically appear to be biased toward kelp sporophytes. Kelp microstages appear to be very vulnerable to changes in environmental conditions (García-Reyes et al., 2022), as these control if and when each stage proceeds to the next, and therefore the overall reproductive success of the kelp species in question. Therefore, it is necessary that we improve our understanding of how kelp microstages will be affected by stressor combinations in a changing climate. In structuring these multiple stressor investigations, researchers should ideally consider ecologically relevant stressor levels and combinations, with a view to how real-world conditions are likely to change in the coming years.
Finally, several studies included in this review have indicated that several kelp species exhibit some degree of inherent resilience to changing environmental conditions (Hollarsmith et al., 2020;Palacios et al., 2021). This appears to be related to genetic variation within kelp species, wherein local adaptation, environmental conditioning, and/or epigenetic responses have resulted in ecotypes specifically resilient to certain environmental conditions (Gerard, 1990;Møller Nielsen et al., 2016;Monteiro, Li, et al., 2019;Müller et al., 2008;Spurkland & Iken, 2012). This may provide a path toward futureproofing kelp forests in climatically vulnerable regions through active interventions. Studies that investigate the potential of experimental transplantation or selective cultivation of resilient genotypes would be useful both with a view toward conservation of wild populations and for increasing efficiency and economic return in a mariculture setting.
In terms of kelp forests in Alaska, based on the trends observed throughout this review, we would expect S. latissima to expand its distributional range throughout the Alaskan region.
This species is relatively warm-adapted (Andersen et al., 2013;Li, Monteiro, et al., 2020) and is also resilient to changes in sediment load and light penetration Picard, Johnson, Ferrario, et al., 2022;Roleda & Dethleff, 2011;Traiger & Konar, 2017), and will therefore be able to persist in warming waters and glacially-influenced areas. Macrocystis pyrifera is also likely to expand northwards and may come to dominate the high-latitude subtidal in wave-influenced areas (Hollarsmith et al., 2020;Le et al., 2022). As cold-adapted species, E. fistulosa and A. marginata are likely to experience range contractions and may disappear from some regions of the Alaskan coastline entirely (Park et al., 2017).

ACK N OWLED G M ENTS
We would like to thank all the researchers and colleagues whose work forms the basis of this review, and specifically Manon Picard and Brooke Weigel for several insightful conversations. We would like to thank both anonymous reviewers for their constructive comments, which contributed greatly to the improvement of this manuscript. Veronica Farrugia Drakard is funded by the Cooperative Institute for Climate, Ocean, and Ecosystem Studies (CICOES), through the CICOES Postdoctoral Program.

DATA AVA I L A B I L I T Y S TAT E M E N T
Data sharing is not applicable as no new data were created or analyzed in this study.